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Biol. Bull. 213: 76-87. (August 2007)
© 2007 Marine Biological Laboratory

Effects of Temperature and UV Radiation Increases on the Photosynthetic Efficiency in Four Scleractinian Coral Species

Christine Ferrier-Pagès1,*, Cécile Richard1, Didier Forcioli2, Denis Allemand1,2, Michel Pichon3 and J. Malcolm Shick4

1 Centre Scientifique de Monaco, Avenue Saint Martin, MC-98000 Monaco
2 UMR 1112 UNSA INRA, Université de Nice-Sophia Antipolis, BP71, F-06108 Nice Cedex 02, France
3 EPHE, Laboratoire des Ecosystèmes aquatiques tropicaux & méditerranéens, Université de Perpignan, 66860 Perpignan Cedex, France
4 School of Marine Sciences, University of Maine, Orono, Maine 04469-5751

To whom correspondence should be addressed: e-mail: ferrier{at}centrescientifique.mc


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Literature Cited
 
Experiments were performed on coral species containing clade A (Stylophora pistillata, Montipora aequituberculata) or clade C (Acropora sp., Pavona cactus) zooxanthellae. The photosynthetic efficiency (Fv/Fm) of the corals was first assessed during a short-term increase in temperature (from 27 °C to 29 °C, 32 °C, and 34 °C) and acute exposure to UV radiation (20.5 W m–2 UVA and 1.2 W m–2 UVB) alone or in combination. Increasing temperature to 34 °C significantly decreased the Fv/Fm in S. pistillata and M. aequituberculata. Increased UV radiation alone significantly decreased the Fv/Fm of all coral species, even at 27 °C. There was a combined effect of temperature and UV radiation, which reduced Fv/Fm in all corals by 25% to 40%. During a long-term exposure to UV radiation (17 days) the Fv/Fm was significantly reduced after 3 days’ exposure in all species, which did not recover their initial values, even after 17 days. By this time, all corals had synthesized mycosporine-like amino acids (MAAs). The concentration and diversity of MAAs differed among species, being higher for corals containing clade A zooxanthellae. Prolonged exposure to UV radiation at the nonstressful temperature of 27 °C conferred protection against independent, thermally induced photoinhibition in all four species.

Abbreviations: FvFm, photosynthetic efficiency • MAA, mycosporine-like amino acid • PAR, photosynthetically active radiation • ROS, reactive oxygen species • UVR, ultraviolet radiation


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Literature Cited
 
Corals are among the most productive organisms in aquatic ecosystems (Falkowski and Raven, 1997) because they host symbiotic dinoflagellates (zooxanthellae), which provide them with large amounts of photosynthates for their energetic requirements (Falkowski et al., 1990). Coral reefs, however, face unprecedented pressures on local, regional, and global scales as a consequence of climate change and anthropogenic disturbances. The responses to such stress are often a decrease in the photosynthetic efficiency of the symbiotic dinoflagellates, as well as bleaching (which involves the mass expulsion of these symbionts, or loss of their pigments (Hoegh-Guldberg, 1999).

Elevated temperatures are suggested to be an important trigger to coral bleaching. A decrease in photosynthetic efficiency is indeed often observed after a heat stress in both cultured zooxanthellae (Iglesias-Prieto et al., 1992; Bhagooli and Hidaka, 2003) and those in hospite (Fitt and Warner, 1995; Warner et al., 1996, 1999; Jones et al., 2000; Bhagooli and Hidaka, 2003; Hill et al., 2004). The loss of efficiency results from an increased sensitivity to photoinhibition (Jones et al., 1998; Hoegh-Guldberg and Jones, 1999) and damage to the D1 protein of photosystem II (Warner et al., 1996, 1999).

Several studies have also implicated solar radiation, including photosynthetically active radiation (PAR) and ultraviolet radiation (UVR, 290–400 nm), as causes of coral stress because tropical corals live in habitats where solar irradiance is extremely high (Shick et al., 1996; Lesser, 2000). UVB (290–320 nm) is known to induce direct damage to DNA via formation of the cyclobutane pyrimidine dimer (CPD) photoproduct (Lyons et al., 1998). The formation of these dimers alters gene expression and DNA replication, and causes genetic mutation. Especially in photosynthetic organisms, solar UV radiation also involves the production of toxic reactive oxygen species (ROS) that subsequently disrupt protein synthesis, cause cellular damage such as in proteins and photosynthetic membranes (Lesser et al., 1990; Lesser, 1997), and induce photoinhibition of photosynthesis (Lesser, 1996). As a consequence, excess PAR was studied with regard to its own short- or long-term detrimental effects on the photosynthesis by the zooxanthellae (Hoegh-Guldberg and Jones, 1999; Brown et al., 2000; Lesser and Gorbunov, 2001; Jones and Hoegh-Guldberg, 2001). UV radiation also severely decreases the photosynthesis in freshly isolated zooxanthellae (Lesser and Shick, 1989; Shick et al., 1995; Lesser, 1996) and those in hospite (Kinzie, 1993; Shick et al., 1995; Lesser and Lewis, 1996). Such damage occurs despite the fact that corals are able to synthesize UV-absorbing compounds, known as mycosporine-like amino acids (MAAs), that have a protective role against UVR (Shick et al., 1995; Dunlap and Shick, 1998; Shick and Dunlap, 2002; Shick, 2004). They also synthesize two enzymes, superoxide dismutase and catalase, which are among the universal defenses against damage from ROS in living tissue (Shick and Dykens, 1985; Richier et al., 2003; Levy et al., 2006).

Large-scale coral bleaching has, however, been ascribed to small increases in sea surface temperature above the long-term summer maximum under bright solar radiation (Hoegh-Guldberg, 1999; Fitt et al., 2001), both temperature and radiation being very high during calm, sunny days in summer (Drollet et al., 1995). Bleaching is indeed exacerbated when corals are exposed to a combination of stresses (Fitt and Warner, 1995; Lesser et al., 1990; D'Croz and Maté, 2002). Few studies have, however, investigated the possibly synergistic effect of an increase in temperature at seasonally high levels of solar radiation (including UVR) on the photosynthetic efficiency of isolated zooxanthellae (Lesser, 1996) or those in hospite (Fitt and Warner, 1995; Lesser and Farrell, 2004; Torregiani and Lesser, 2007). Such an investigation is an essential step in understanding and predicting the fate of coral reefs under conditions of global change. It has been shown, in corals exposed to an elevated temperature of 32 °C, that solar radiation, and especially UVB, inhibits photosynthesis by damaging photosystems and decreasing carbon fixation (Fitt and Warner, 1995; Lesser, 1996).

The aim of this study was therefore to experimentally assess the short-term effect of an increase in (i) temperature alone, (ii) UVR alone, and (iii) temperature and UVR together, on the photosynthetic efficiency in four coral species (Pavona cactus, Stylophora pistillata, Montipora aequituberculata, and Acropora sp.). Interspecific comparisons are important because corals may react differently to a change in their environmental conditions resulting from different levels of oxidative stress (Lesser, 1996), zooxanthella genotypes (Rowan et al., 1997), pigments (Hoegh-Guldberg and Jones, 1999), tissue thickness (Loya et al., 2001), and colony shape (Glynn, 1993). The photosynthetic system's potential for recovery after stress was also examined over several days, and the genetic identity of the zooxanthellae contained by each coral species was investigated. In a second experiment, we also followed the effect of a long-term increase (17 days) in UV radiation alone on the photosynthetic efficiency of the same coral species. The levels of individual MAAs at the beginning and at the end of the experiment were measured.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Literature Cited
 
Experiments were performed in the laboratory using nubbins of four scleractinian corals: Stylophora pistillata (Esper, 1797), Pocilloporidae, branching colonies; Pavona cactus (Lamarck, 1801), Agariciidae, foliacious colonies; Montipora aequituberculata (Bernard, 1897) and Acropora sp., Acroporidae, respectively unifacial and branching platelike colonies. The complete identification of Acropora sp. was not possible, but skeletons are available. Nubbins were maintained without UV radiation in the aquaria of the laboratory of the Centre Scientifique de Monaco. They were fed once a week with Artemia salina nauplii, except during experiments, when they were not fed. Nubbins from each species were prepared by cutting portions of at least three parent colonies with surgical bone forceps. The nubbins were ready for use when the animal tissue entirely covered the skeleton (ca. 3 weeks)

Short-term effect of UVR and temperature
To study the short-term effect of a combination of UVR and temperature, 200 nubbins (50 from each species) were prepared and maintained, on nylon nets, for 3 weeks, in five 30-1 aquaria continuously supplied with seawater. A PAR irradiance of 300 ± 20 µmol photons m–2 s–1 (photoperiod 12:12 h) was provided by 400-W metal halide lamps (Philips, HPIT). Irradiance was measured using a 4{pi} quantum sensor (Li-Cor, LI-193SA). Temperature was set at 27 °C (precision: ± 0.1 °C) and was logged at 10-min intervals using a Seamon temperature recorder. These five aquaria will be referred to as Control tanks.

In addition, four 10-1 tanks were prepared for the "stress" experiments, with the same arrangement and PAR as described above. Two tanks received UV radiation in addition to PAR (hereafter called PAR/UV tanks), while the two other tanks (hereafter called PAR tanks) remained shaded from UV by a UV-opaque Lee 226 polycarbonate cutoff filter. For the PAR/UV tanks, UV radiation was provided by two UV-340 fluorescent lamps (Q-Panel Lab Products), giving a UVA fluence of about 20.5 W m–2 and a UVB fluence of about 1.2 W m–2 (Shick, 2004). These levels are similar to those measured in the field at 1–2 m depth (Shick et al., 1996). Higher levels of incident UV radiation can be measured at the surface at midday (e.g., 39 and 2.2 W m–2 UVA and UVB, respectively; Torregiani and Lesser, 2007). Four experiments were performed in these 10-1 tanks to test the effect of four temperatures (27 °C, 29 °C, 32 °C, and 34 °C), in the presence or absence of UV radiation, on the photosynthetic efficiency of the corals. The effect of temperature alone was tested in the tanks that did not receive UV radiation. The effect of UV radiation alone was tested in the tanks maintained at 27 °C, which is the "normal" (control) temperature at which corals were maintained. The interacting effect of temperature and UV was tested in the other treatments (UV and 29 °C, 32 °C, 34 °C). Such high temperatures were chosen because they occur in situ during bleaching events (Glynn, 1993; Jones, 1997; Berkelmans and Willis, 1999).

For each experiment, 12 nubbins from each species were randomly taken from the Control tanks and transferred to the PAR/UV and PAR tanks (3 nubbins per species and per tank). Temperature was then gradually increased (0.2 °C per minute) and maintained at the stated value for 5 h (as well as UV radiation), as was done in most of the previous experiments that tested a temperature stress (Bhagooli and Hidaka, 2003, 2004; Yakovleva and Hidaka, 2004a; Hill et al., 2004). At the end of the incubation period, corals were returned to the Control tanks. The Fv/Fm of each nubbin was measured in the Control tank just before the stress (T0), in the experimental tanks at the end of the 5-h stress (TF), and again in the Control tank after 24 h of recovery (TR).

Long-term effect of UVR
This second experiment was designed to assess the long-term effect of UV radiation on the photosynthetic efficiency of the corals. The accumulation of MAAs was also monitored. Thirty-eight nubbins of the four coral species were prepared. After healing, they were randomly divided among four 20-1 tanks that were continuously supplied with seawater at 27 °C and received a PAR irradiance of 300 ± 20 µmol photons m–2 s–1 (photoperiod 12:12 h). Two tanks remained as Control tanks, and the two other tanks additionally received the same UV irradiance as described in the previous section for 5 h every day for 17 days (UV tanks). The Fv/Fm of each nubbin was measured at the start of the experiment and after 4, 8, 11, 14, and 17 days. At the end of the incubation, six nubbins of each species were sampled in the Control and UV tanks for determination of MAAs and chlorophyll a (described in the next section). The remaining nubbins were used in temperature-stress experiments. For this purpose, the seawater temperature for each treatment (Control and UV tanks) was successively increased to 29, 32, or 34 °C over 5 h, and the response of four nubbins (in each condition and each species) was monitored. The Fv/Fm of each nubbin was measured immediately before and at the end of the temperature stress and after 24 h of recovery at 27 °C.

Measurement of chlorophyll fluorescence
During all experiments, the maximal quantum yield (dark-adapted Fv/Fm) of zooxanthellae in hospite was measured for each nubbin by using an underwater pulse amplitude modulation fluorometer (a DIVING PAM; Walz, Germany). This parameter gives information on the photosynthetic efficiency of the coral (Schreiber, 2004). A micromanipulator was used to place the optical fiber (8 mm in diameter) of the fluorometer 5 mm above the coral nubbin. The optical head was surrounded by a black neoprene holder to keep a constant distance (5 mm) between the sample and the optic fiber. The initial fluorescence (F0) was measured by applying a weak pulsed red light (LED 650 nm, 0.6 kHz, 3 µs). A saturating pulse of bright actinic light (8000 µmol photons m–2 s–1, width 800 ms) was then applied to give the maximal fluorescence value (Fm). Variable fluorescence (Fv) was calculated as Fm – F0 and maximal quantum yield as Fv/Fm.

Determination of MAAs and chlorophyll a
Nubbins from each species were sampled in the Control and UV tanks after 14 days of incubation. They were extracted in HPLC-grade methanol and analyzed for MAAs (Shick, 2004). Prior to cleaning the methanolic extracts on C-18 Sep-Pak plus cartridges (Waters), chlorophyll a was quantified with a spectrophotometer, using the extinction coefficient of 0.0191 m2 (mg chlorophyll a)–1 at 665 nm (Stramski and Morel, 1990). All data were expressed per milligram of protein, determined as in Grover et al. (2002). Normalizing data per skeletal surface area was impossible because measurement of area in species such as Pavona cactus, which is foliacious, is very difficult and imprecise.

Analysis of zooxanthellae
DNA was extracted following LaJeunesse (2002). Clades were determined by PCR-RFLP on the nuclear ribosomal small- and large-subunit coding DNA (Rowan and Powers, 1991; Savage et al., 2002). The small-subunit coding sequence was amplified using the universal (ss3) and zooxanthellae-specific (ss5Z) primers (Rowan and Powers, 1991). PCR reactions were performed on 10 µl of a 1/100 dilution of the DNA extracts, with a final concentration of 1 x PCR reaction buffer (Invitrogen), 2 mmol l–1 MgCl2, 0.5 µmol l–1 of each primer, 80 nmol l–1 dNTPs and 1.5 U of Platinum Taq DNA polymerase (Invitrogen). PCR was performed on an Eppendorf Mastercycler gradient with the following temperature cycle: a 2-min initial denaturation at 94 °C, followed by 40 cycles of 45 s at 94 °C, 1 min at 53 °C, and 2 min at 72 °C, and 7 min of final elongation at 72 °C. PCR products were checked by electrophoresis. Clades were identified by a TaqI restriction of the PCR product (Rowan and Powers, 1991), performed overnight at 65 °C, with 8 µl of the PCR amplification product, 5 U of TaqI enzyme (New England Biolabs), 1 x final concentration of TaqI restriction Buffer (NEB) and 10 µg ml–1 of bovine serum albumin. Restriction products were run on a 2% agarose gel electrophoresis in 2x Tris-acetate-EDTA buffer. Clade-specific restriction profiles were identified (Savage et al., 2002). To further distinguish "temperate A" from "tropical A" clade (Savage et al., 2002), the ribosomal large-subunit coding sequence was amplified using the specific primers Ls1-5 and Ls1-3. PCR reactions were performed as previously described, except for the temperature cycle, which was as follows: 3 min at 95 °C, followed by 45 cycles of 45 s at 92 °C, 45 s at 63 °C, 1 min at 72 °C, and finally 7 min at 72 °C. The "temperate A" was separated from the "tropical A" clade by digesting this PCR product by the DdeI restriction enzyme (Savage et al., 2002). DdeI restrictions were performed overnight at 37 °C in 20 µl of total reaction mixture, with 8 µl of the PCR amplification product, 5 U of DdeI enzyme (New England Biolabs), and a final concentration of 1x DdeI restriction buffer (NEB).

Statistical analyses
In the short-term experiment, comparisons between treatments and species were tested using one- or multiple-factor ANOVAs. In significant analyses, data were compared with the Bonferroni/Dunn post hoc test. Data obtained at each temperature, with and without UV radiation, were compared using an unpaired Student's t-test. In the long-term experiment, temporal differences in Fv/Fm were tested using a one-factor ANOVA and the Bonferroni/Dunn post hoc test.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Literature Cited
 
Short-term effect of UV radiation and temperature
Under control conditions, that is, at 27 °C without UV radiation, photosynthetic efficiency (Fv/Fm) for each coral species remained constant during the 24-h incubation (Fig. 1), and equal to 0.65 ± 0.03 (mean ± SD) for all species except Montipora aequituberculata, for which the value was slightly lower (0.55 ± 0.02). A short-term increase in temperature alone, from 27 °C to 34 °C (Fig. 1, –UV) had no significant effect on the Fv/Fm of zooxanthellae of Acropora sp. and Pavona cactus (ANOVA, P = 0.09 and 0.39, respectively). However, Fv/Fm measured at 34 °C was significantly lower than the values obtained at the other temperatures for M. aequituberculata (ANOVA, P = 0.01) and Stylophora pistillata (ANOVA, P < 0.001). For the latter corals, the maximum quantum yield recovered its initial value after 24 h in the Control tanks.


Figure 1
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  		Figure 1. Short-term experiment. Maximum quantum yield (Fv/Fm) of zooxanthellae in hospite measured at the end of 5-h incubation at 27, 29, 32, and 34 °C. Corals were maintained either under UV radiation (+UV) or without (–UV). Data are mean and standard deviation of 5 nubbins. White and pale grey bars correspond to the Fv/Fm value measured immediately before and at the end of the temperature stress, respectively; dotted bars represent the recovery value, measured 24 h after the stress.

 
The effect of UV radiation alone (without the additional temperature effect) was assessed by comparing the corals incubated at 27 °C –UV with those at 27 °C +UV (Table 1). For all coral species except Acropora sp., UV radiation alone had a significant negative impact on the maximum quantum yield, with a decrease of about 15% in the Fv/Fm of the three coral species. Table 1 and Figure 1 also show that the values of Fv/Fm measured under UV radiation at the different temperature treatments were always significantly lower than the Fv/Fm measured at the same temperature treatments but without UV.


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  		Table 1 Results of unpaired t-tests comparing, for each species, the Fv/Fm measured at the end of a 5-h temperature increase (TF) in corals receiving UV radiation (+UV) or not (–UV)

 
There was also an interacting effect of temperature and UV radiation on the Fv/Fm for three out of the four coral species (Table 2 and Fig. 1). As a result, under UV exposure the Fv/Fm of Acropora sp. continuously declined (by more than 40%) between 29 °C and 34 °C (Table 2), and 50% of the nubbins died 24 h after the stress. Nubbins recovered their initial Fv/Fm value after 24 h back in control conditions, except those that died at 34 °C (Table 2, Fig. 1). P. cactus showed a significantly reduced (by 25%) Fv/Fm at temperatures higher than 27 °C (Table 2, Fig. 1), and S. pistillata presented the same decrease at 32 °C and 34 °C. These corals did not recover their initial Fv/Fm after experiencing a shock of 34 °C +UV (t-test, P < 0.05). Only M. aequituberculata showed no combined effect of UV and temperature (the effect of UV was constant with the increase in temperature, with about an 18% decrease for all temperatures, Table 2). Moreover, all nubbins recovered their initial Fv/Fm after the stress (Fig. 1, t-test, P > 0.05).


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  		Table 2 Short-term experiment: results of two-factor ANOVA testing, for each species, the effect of time (T0, TF, TR) and treatment (temperature + UV radiation increase) on the Fv/Fm; * denotes significant

 
Long-term effect of UV radiation
Figure 2 shows the Fv/Fm in corals maintained for 17 days at 27 °C under ultraviolet radiation. There was a significant decrease in the maximum quantum yield after the first 5 days of incubation for Acropora sp. (ANOVA, df = 4, F = 8.68, P < 0.001), P. cactus (df = 4, F = 30.94, P < 0.001), and S. pistillata (df = 4, F = 13.67, P < 0.001). This yield did not recover its initial value at the end of the incubation. Conversely, the Fv/Fm in nubbins remaining under control conditions (without UV) did not change (Fig. 2) during the whole incubation time (ANOVA, P > 0.05).


Figure 2
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  		Figure 2. Long-term experiment. Maximum quantum yield (Fv/Fm) measured during 17 days of incubation (i) under UV radiation at 27 °C (black lozenges) and (ii) without UV radiation at 27 °C (white squares). Data are mean and standard deviation for 5 nubbins.

 
Measurements of MAAs in the tissue after 14 days of incubation under UV radiation are represented in Figure 3. They are normalized to the amount of protein to be comparable between species, since this amount did not change during the incubation (ANOVA, P < 0.005). The two-factor ANOVA showed that all coral species had produced significantly higher amounts of MAAs compared with the controls (df = 1, F = 103.01, P < 0.001) and that production of MAAs was different between species (df = 3, F = 4.25, P = 0.022). S. pistillata and M. aequituberculata indeed increased by about 8 times their MAA content compared with the control, whereas P. cactus and Acropora sp. increased it by 3 to 4 times, with final concentrations in the former two species being about twice those in the latter two species. MAA composition differed among the coral species. Mycosporine-glycine was accumulated by all corals and was the main constituent in three out of the four coral species (Fig. 3). Shinorine, porphyra-334, palythine, and palythine-serine were the next most abundant MAAs in all coral species except for P. cactus, which did not contain shinorine. S. pistillata contained two additional MAAs (palythine-serine sulfate and mycosporine-NMA:serine), while M. aequituberculata uniquely had another three (asterina-330, usujirene, and palythene). After 14 days of incubation, there was no significant difference in chlorophyll a concentration between corals in the control and UV tanks, except for Acropora sp. (Fig. 4), in which this pigment significantly decreased by more than 50% (t-test, P < 0.001).


Figure 3
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  		Figure 3. MAAs accumulated after 14 days of incubation at 27 °C in Control (–UV) and UV (+UV) tanks. 1, Palythine-serine-sulfate; 2, Mycosporine-glycine; 3, Shinorine; 4, Porphyra-334; 5, Palythine or Palythine-serine; 6, Mycosporine-NMA:serine; 7, Usujirene; 8, Palythene.

 

Figure 4
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  		Figure 4. Concentration of chlorophyll a (µg (mg protein)–1) in corals sampled in the Control (–UV) and UV tanks (+UV) after 14 days of incubation at 27 °C. Data are mean and standard deviation for 3 nubbins. The asterisk indicates a significant difference between the two treatments.

 
A 5-h temperature stress applied after the corals had been maintained for 17 days under UV produced no significant effect on Fv/Fm (Fig. 5, ANOVA, P = 0.11, 0.25, 0.87, and 0.07 for S. pistillata, P. cactus, M. aequituberculata, and Acropora sp., respectively). Conversely, control corals previously maintained at 27 °C in the absence of UV radiation presented the same significant UV-related decreases in Fv/Fm seen in Figure 1 when acutely exposed to elevated temperatures (results not shown).


Figure 5
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  		Figure 5. Long-term experiment. Maximum quantum yield (Fv/Fm) of zooxanthellae in hospite measured at the end of 5 h incubation at 27, 29, 32, and 34 °C. Corals previously were maintained for 17 days under UV radiation at 27 °C. Data are mean and standard deviation for 5 nubbins. White and pale grey bars correspond to the Fv/Fm value measured before and at the end of the temperature stress, respectively; dotted bars represent the recovery value, measured 24 h after the stress.

 
Zooxanthellae clade identification
All PCR products were of the expected size, without contamination by residual host genomic DNA (data not shown). The TaqI restriction profiles obtained after electrophoresis showed that Acropora sp. and P. cactus contained zooxanthellae belonging to clade C, whereas S. pistillata and M. aequituberculata contained clade A zooxanthellae. No "temperate A" zooxanthellae were found in these corals after DdeI restriction of the large ribosomal subunit (data not shown).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Literature Cited
 
This study highlights the photosynthetic response of zooxanthellae in symbiosis with four scleractinian corals to an acute increase in seawater temperature, alone or in combination with an acute exposure to UV radiation. The combined effect of an elevation in temperature and exposure to UV radiation caused the highest depression of photosynthesis in the four corals tested. Prior acclimation to UV radiation at a nonstressful temperature changed the subsequent response to temperature increase alone.

Levels of UVA and UVB radiation used in this experiment were similar to those measured in the field at 1–2 m depth (Shick et al., 1996). Their effect was tested on corals that were maintained in aquaria for several months under UV-shielded metal halide lamps and that contained very small amounts of MAAs in their tissue (see Fig. 3, as well as Shick, 2004). Their acute response can therefore be compared with the response of corals living in deep water.

A short-term increase in temperature alone had no significant effect on the photosynthetic efficiency of Pavona cactus and Acropora sp.; in the other two species it induced, at 32 and 34 °C, only a transient inhibition of photosynthesis (a decrease of 10% to 12% compared with the control values). This inhibition of photosystem II can be considered as dynamic (Gorbunov et al., 2001) since it recovers on a timescale of minutes to hours, as measured after 24 h in this study. The two species showing the decrease in their maximum quantum yield with temperature, Stylophora pistillata and Montipora aequituberculata, are also the less thermally resistant species in another experiment (Yakovleva and Hidaka, 2004a), and are also generally considered to be susceptible to bleaching (Loya et al., 2001). A difference in the genetically based adaptative capabilities of the zooxanthellae was suggested to explain the different coral responses (La Jeunesse et al., 2003; Yakovleva and Hidaka, 2004a), since temperature can affect the ultrastructural integrity of the thylakoid membranes of some heat-sensitive clades, leading to an uncoupling of photosynthetic energy transduction (Tchernov et al., 2004). In this study, S. pistillata and M. aequituberculata indeed both contained clade A zooxanthellae, while the two other "resistant" species contained clade C zooxanthellae. The thermal tolerances of these two clades remain, however, an open question, since it was first suggested that, conversely to our observations, clade A was more thermally resistant than clade C (Rowan et al., 1997), but it was then shown that different types within a clade could present different tolerances to environmental factors (LaJeunesse et al., 2003; Ulstrup and van Oppen, 2003; Tchernov et al., 2004). It was finally concluded that there was no simple correlation between the symbiont types and the level of bleaching of individual colonies (van Oppen et al., 2005; Ulstrup et al., 2006), suggesting that symbiont polymorphism does not rule out some contribution of genetic differences among hosts or some acclimatization of hosts to high temperatures (Bhagooli and Hidaka, 2004).

This study highlights a strong interaction of temperature and UV radiation in the photoinhibition of the photosynthetic apparatus of the zooxanthellae, in three out of the four coral species (Table 2). Indeed, except in M. aequituberculata, the depression of the maximum quantum yield of all corals ranged from 0% to 14% during an increase in temperature or exposure to UV radiation alone, but reached a 30% to 50% decrease when a temperature of 34 °C was combined with an acute exposure to UVR. Such inhibition of photosynthesis has already been observed during in situ experiments in which corals were exposed to high temperature and unfiltered solar radiation (Fitt and Warner, 1995; Lesser and Farrell, 2004). The present results also show different responses of the coral species to the combined stresses, since the maximum quantum yield of Acropora sp. and S. pistillata continuously decreased with the elevation in temperature, while the yield of P. cactus remained at a constant value from 29 to 34°C. Finally, in M. aequituberculata, the decrease in Fv/Fm obtained with UVR was not exacerbated by an elevation in temperature. Exposure to UVR might directly affect photosynthesis by absorbing excessive energy, causing molecular damage (see review in Hanelt et al., 2003), or even inducing formation of ROS, reactive oxygen species (Lesser, 1996, 1997). ROS both inhibits the biosynthesis of and damages the D1 protein (Lesser and Farrell, 2004; Nishiyama et al., 2001) and Rubisco (Asada and Takahashi, 1987). These fluxes of ROS, added to those arising from sink-limited photoinhibition, overwhelm host and algal antioxidant defenses, resulting in damage to both light and dark reactions (Lesser and Farrell, 2004).

The second part of the present study consisted of testing the effect of an acute increase in temperature on corals previously exposed for 17 days to UV radiation (Fig. 2). After the first 3 days of exposure, the photosynthetic efficiency of all coral species was significantly reduced (13% for M. aequituberculata and, on average, 24% for the other three species). In situ experiments demonstrated the same photosynthetic inhibition when deep corals were transplanted to surface waters (Masuda et al., 1993; Shick et al., 1995), or when shallow-water corals were exposed to midday radiation (Yakovleva and Hidaka, 2004a) or to full sunlight (Jones and Hoegh-Guldberg, 2001; Gorbunov et al., 2001). Mechanisms involved could include the direct effects of UV, as well as production of ROS, with the cellular targets described above. Despite this initial reduction in the maximum quantum yield down to a value of 0.45–0.40, no further decrease in the photosynthetic efficiency was observed during the following 14 days of incubation, suggesting the operation of some protective mechanisms. Corals exposed to UV radiation indeed synthesized large amounts of MAAs (4 to 8 times the concentration measured in control corals). In S. pistillata, synthesis of MAAs occurred rapidly, within several days after initial exposure to UVR (Shick et al., 1999); thereafter these MAAs may have acted as potent UV sunscreens, protecting corals from UV-photoinhibition, as already observed during in situ experiments (Shick et al., 1995; Masuda et al., 1993) or in free-living dinoflagellates (Neale et al., 1998). Production of MAAs might have also prevented bleaching, since chlorophyll a content did not decrease during the incubation in any coral species except Acropora sp. (Fig. 4).

It must be noted, however, that no coral species recovered its initial Fv/Fm value, even 17 days after the start of the experiment and after having accumulated high levels of MAAs in the tissue; this suggests that a chronic inhibition had occurred during the first days and that the damage could not be easily repaired while the corals remained under stress. For example, nitrogen limitation in starved colonies of S. pistillata during exposure to UV radiation restricted their accumulation of MAAs (Shick et al., 2005), and damage repair might have been similarly restricted in the present experiments if MAA biosynthesis and damage repair compete for nitrogen during stress (also see Gleason, 2001).

In the present experiment, the four species accumulated different concentrations, as well as different compositions, of MAAs after 17 days under UV radiation. Acropora sp. and P. cactus were the two coral species containing the lowest amount (at 42 and 35 nmol mg–1 of protein) and diversity (from two to four) of MAAs. The primary Symbiodinium MAA (sensu Shick, 2004), mycosporine-glycine, was the most abundant (87% and 95%, respectively, of the total). A predominance of this MAA was also found in other species of Acropora (A. palmata and A. cervicornis: Banaszak et al., 2006) and Pavona (P. divaricata: Yakovleva and Hidaka, 2004b). Conversely, S. pistillata and M. aequituberculata contained concentrations of MAAs 2 times higher (ca. 80 nmol mg–1 of protein), and a greater diversity of them (six to seven different MAAs). This high MAA diversity in Stylophora and Montipora species was observed previously (Shick et al., 1999; Yakovleva et al., 2004; Yakovleva and Hidaka, 2004b). S. pistillata also contained a large amount (82% of total MAAs) of primary Symbiodinium MAAs, but divided in equal proportions among mycosporine-glycine, porphyra-334, and shinorine. Finally, M. aequituberculata differed notably from the three other species because it contained only 28%–29% of primary MAAs (in equal proportion among mycosporine-glycine, shinorine, and porphyra-334), and therefore more than 70% of its MAAs were secondary products such as palythine, usujirene, and palythene.

The difference in MAA concentration and diversity may reflect a genotypic difference among zooxanthellae, or among hosts. Indeed, whereas primary Symbiodinium MAAs are produced by zooxanthellae, secondary MAAs may be produced in the host animal by conversion of primary MAAs (Shick, 2004). Therefore, the qualitative differences in the complement of MAAs between S. pistillata and Montipora sp. might result from their hosting different types of clade A zooxanthellae or from using different pathways of MAA conversion. The presence, in the host tissue, of photoprotective molecules other than MAAs, as well as the morphology of the coral skeleton, may also contribute to the difference in MAA production (Banaszak et al., 2006), since these two factors can change the light environment of the symbionts. It is noteworthy that both corals containing clade C zooxanthellae were those accumulating the lowest amount of MAAs, mainly composed of primary Symbiodinium MAAs.

Prolonged (17-day) exposure to UV radiation at the nonstressful temperature of 27 °C also conferred protection against independent, thermally induced photoinhibition in all four species. This was indicated by the unchanging Fv/Fm of all UV-acclimated corals during an elevation of temperature to 34°C. This is the first time that such protection has been demonstrated experimentally. Some similar conclusions may be drawn from an in situ study showing that parts of colonies that were regularly exposed to the highest solar radiation were more thermally tolerant than areas that were less exposed (Brown et al., 2002). It has also been observed that shallow-water corals were more thermally resistant than deeper living ones, because they possessed a higher protection due to their constant exposure to a high level of solar radiation (Hoegh-Guldberg and Salvat, 1995). In those previous studies, however, it is unknown whether it was the PAR or UVR component of sunlight, or both, that induced some defense mechanisms that protected photosynthesis during acute thermal stress, particularly if the combination of thermal and solar stress involved ROS formation. Major defense mechanisms that might have been induced in our experiment during exposition to UV radiation include antioxidant enzymes (Shick et al., 1995; Brown et al., 2000; Lesser and Farrell, 2004), pigments (Salih et al., 2000; Ambarsari et al., 1997), and MAA production (Dunlap and Yamamoto, 1995; Yakovleva et al., 2004). Among MAAs, mycosporine-glycine, synthesized by all four coral species, has some antioxidant activity (Dunlap and Yamamoto, 1995; Yakovleva et al., 2004), as does the metabolically related 4-deoxygadusol (Dunlap et al., 2000; Shick and Dunlap, 2002). Mycosporine-glycine is indeed a predominant MAA in zooxanthellate anthozoan symbioses of the Great Barrier Reef and Caribbean reefs (Shick et al., 1991, 1995; Gleason and Wellington, 1995; Banaszak et al., 2006), which may be related to both its UVB screening and its antioxidant function. The bleaching susceptibility of corals therefore depends on their previous history as well as on the capacity for upregulating their defenses.

Results obtained in this study show that there is a complex set of interactions between the environmental factors that can lead to different coral responses to a stress. An abrupt increase in seawater temperature can have a negative impact on coral photobiology when it is combined with an acute exposure to UV radiation, but long-term exposure to ambient UV radiation at nonstressful temperatures may also protect corals from an acute thermal stress. Moreover, different coral species do not have the same physiological response to changes in their environment.


   Acknowledgments
 
This research was supported by the Centre Scientifique de Monaco, the University of Nice–Sophia Antipolis, and U.S. NSF grant OCE 9907305. A special thanks to Drs. Marcel Babin and Yannick Huot (Observatoire Océanologique de Villefranche) for their valued help.


   Footnotes
 
Received 28 September 2006; accepted 29 April 2007.


   Literature Cited
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
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